Integrated multi-omics framework of the plant response to jasmonic acid

• Published in: Nature plants Vol. 6; no. 3; pp. 290 - 302
• Main Authors: Zander, Mark, Lewsey, Mathew G., Clark, Natalie M., Yin, Lingling, Bartlett, Anna, Saldierna Guzmán, J. Paola, Hann, Elizabeth, Langford, Amber E., Jow, Bruce, Wise, Aaron, Nery, Joseph R., Chen, Huaming, Bar-Joseph, Ziv, Walley, Justin W., Solano, Roberto, Ecker, Joseph R.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.03.2020; Nature Publishing Group
• Subjects: 38/39; 45/15; 45/91; 631/208/212; 631/449/1741/2671; 631/449/2675; 96/95; Alternative splicing; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics; Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism; Biomedical and Life Sciences; Chromatin remodeling; Crosstalk; Cyclopentanes - metabolism; Environmental effects; Gene expression; Gene Expression Profiling; Gene Regulatory Networks; Genomes; Hormones; Jasmonic acid; Life Sciences; Mutants; Oxylipins - metabolism; Phosphoproteins - metabolism; Phosphorylation; Plant Growth Regulators - genetics; Plant Growth Regulators - metabolism; Plant Sciences; Proteins; Proteomics; Regulatory mechanisms (biology); Signal Transduction; Signaling; Splicing; Trans-Activators - genetics; Trans-Activators - metabolism; Transcription factors; Transcriptomes; La Jolla California; Victoria Australia; California; Australia; United States > US
• ISSN: 2055-0278; 2055-0278
• DOI: 10.1038/s41477-020-0605-7

Understanding the systems-level actions of transcriptional responses to hormones provides insight into how the genome is reprogrammed in response to environmental stimuli. Here, we investigated the signalling pathway of the hormone jasmonic acid (JA), which controls a plethora of critically important processes in plants and is orchestrated by the transcription factor MYC2 and its closest relatives in Arabidopsis thaliana . We generated an integrated framework of the response to JA, which spans from the activity of master and secondary regulatory transcription factors, through gene expression outputs and alternative splicing, to protein abundance changes, protein phosphorylation and chromatin remodelling. We integrated time-series transcriptome analysis with (phospho)proteomic data to reconstruct gene regulatory network models. These enabled us to predict previously unknown points of crosstalk of JA to other signalling pathways and to identify new components of the JA regulatory mechanism, which we validated through targeted mutant analysis. These results provide a comprehensive understanding of how a plant hormone remodels cellular functions and plant behaviour, the general principles of which provide a framework for analyses of cross-regulation between other hormone and stress signalling pathways. Five genome-wide approaches are integrated to give a comprehensive picture of jasmonic acid signalling networks in Arabidopsis . New genes, validated by mutant analysis, and important connections with other pathways are revealed.